Cortical-basal ganglia (CBG) circuits are critical for normal motor and reinforcement learning, and accordingly are a major site of psychiatric and neurological pathology, including schizophrenia and addictions. However, because of their cellular and circuit complexity, and the broad suite of behaviors they control, many basic questions about the link between neural signals in these circuits and behavior remain unanswered. Songbirds provide a powerful model in this regard, because they have a specialized CBG loop, the anterior forebrain pathway (AFP), devoted to a well-defined learned behavior, song. Recent studies in songbirds, including our own work from the last grant cycle, have suggested an important new function for CBG circuits, the active generation of behavioral variability important for learning. Consistent with this, LMAN, the 'cortical'outflow nucleus of the AFP, carries both a temporally structured signal related to song, and trial-by-trial variability around that signal. Moreover, both neural and behavioral variability can markedly decrease when birds are in a social, 'performance'context, possibly in response to midbrain dopamine (DA) release. We will now ask how and where neural variability and its underlying pattern emerge in the song network, and how the different stages of the AFP contribute to these signals and to song in both juveniles and adults, using recordings of multiple neurons in combination with behavioral and pharmacological manipulations of the AFP. Our first aim will study the first nucleus in the circuit, the striato-pallidal Area X, during both alone ('undirected') and female-directed singing, and will test possible sources of context-dependent variation by acutely blocking LMAN recurrent inputs or DA receptors. Our second aim will further test the importance of different stages of the AFP by examining LMAN activity in response to manipulations of Area X, and of its thalamic target DLM. Finally, we will test how both variability and patterned signals emerge and evolve in LMAN during learning in juvenile birds, and how they respond to social cues. The systematic dissection of circuit function possible in this system should shed light not only on normal learning, but on the many diseases of these circuits, whose symptoms often include too little or too much variability. PUBLIC HEALTH RELEVANCE: Cortical-basal circuits are the complex site of many disabling neuropsychiatric disorders. A mechanistic understanding of how these circuits can change their signaling, and the resulting song, both in adults and during learning, in response to manipulations of social context and of different stages of the circuit, has the potential to provide new insights into dysfunction in these areas, and to suggest new treatment strategies.